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1 Caesarean delivery rates and regnancy outcomes: the 0 WHO global survey on maternal and erinatal health in Latin America José Villar, Eliette Valladares, Daniel Wojdyla, Nelly Zavaleta, Guillermo Carroli, Alejandro Velazco, Archana Shah, Liana Camodónico, Vicente Bataglia, Anibal Faundes, Ana Langer, Alberto Narváez, Allan Donner, Mariana Romero, Sofia Reynoso, Karla Simônia de Pádua, Daniel Giordano, Marius Kublickas, Arnaldo Acosta, for the WHO 0 global survey on maternal and erinatal health research grou* Summary Background Caesarean delivery rates continue to increase worldwide. Our aim was to assess the association between caesarean delivery and regnancy outcome at the institutional level, adjusting for the regnant oulation and institutional characteristics. Methods For the 0 WHO global survey on maternal and erinatal health, we assessed a multistage stratified samle, comrising 24 geograhic regions in eight countries in Latin America. We obtained individual data for all women admitted for delivery over 3 months to institutions randomly selected from of 4 identified institutions. We also obtained institutional-level data. Findings We obtained data for of 6 46 deliveries (9% coverage). The median rate of caesarean delivery was 33% (quartile range 24 43), with the highest rates of caesarean delivery noted in rivate hositals (%, 43 7). Institution-secific rates of caesarean delivery were affected by rimiarity, revious caesarean delivery, and institutional comlexity. Rate of caesarean delivery was ositively associated with ostartum antibiotic treatment and severe maternal morbidity and mortality, even after adjustment for risk factors. Increase in the rate of caesarean delivery was associated with an increase in fetal mortality rates and higher numbers of babies admitted to intensive care for 7 days or longer even after adjustment for reterm delivery. Rates of reterm delivery and neonatal mortality both rose at rates of caesarean delivery of between % and %. Interretation High rates of caesarean delivery do not necessarily indicate better erinatal care and can be associated with harm. Introduction Rates of caesarean delivery have risen from about % in develoed countries in the early 9s to more than 0% in some regions of the world in the late 9s. 6 Many factors have contributed to this rise, including imroved surgical and anaesthetic techniques, reduced risk of ost-oerative comlications, demograhic and nutritional factors, 7,8 roviders and atients ercetion of the safety of the rocedure, 9 obstetricians defensive ractice, changes in health systems, and atient demand. 2,3 Caesarean delivery is thought to rotect against urinary incontinence, rolase, and sexual dissatisfaction, increasing its aeal. 4, Finally, the rise in numbers of women oting for a caesarean might also be affected by obstetricians defence of women s rights to choose their method of delivery. 6 Medical strategies, such as mandatory second oinion before doing a caesarean section, have not reduced the numbers of caesarean deliveries, 7 and a randomised trial to comare erinatal outcomes and satisfaction of caesarean delivery on demand for all women versus caesarean delivery only when clinically indicated is being contemlated. 8 Before such ractice can be assessed and an aroriate trial designed, however, the otimum roortion of caesarean deliveries for any articular institution, based on the risk rofile of that institution s regnant oulation, needs to be identified. 3,9, Our aim was to assess the association between rates of caesarean delivery and maternal and erinatal outcomes at the institutional level. Methods Poulation We designed the 0 WHO global survey on maternal and erinatal health to exlore the relation between rates of caesarean delivery and erinatal outcomes in the medical institutions of eight randomly selected countries in the region of the Americas, using a multistage stratified samling rocedure. We obtained data between Set, 04, and March, 0. After country selection, we identified a reresentative samle of geograhic areas within each country and, within these geograhic areas, a reresentative samle of care units. We selected countries with a robability roortional to the oulation of the country, rovinces with a robability roortional to the oulation of the rovince, and health institutions with a robability roortional to the number of deliveries er year. Here, we resent results from the eight countries in Latin Lancet 06; 367: See Comment age 796 Published Online May 23, 06 DOI:.6/S (06)684-7 *All listed at end of reort UNDP/UNFPA/WHO/World Bank Secial Programme of Research, Develoment and Research Training in Human Reroduction, Deartment of Reroductive Health and Research, WHO, 2 Geneva 27, Switzerland (J Villar MD, A Shah MSc); Universidad Nacional Autónoma de Nicaragua, León, Nicaragua (E Valladares MD); Centro Rosarino de Estudios Perinatales, Rosario, Argentina (D Wojdyla MSc, G Carroli MD, L Camodónico MSc, D Giordano BS); Instituto de Investigación Nutricional, Lima, Peru (N Zavaleta MD); Hosital Docente Ginecobstétrico América Arias, La Habana, Cuba (A Velazco MD); Deartment of Obstetrics and Gynecology, Hosital Nacional de Itauguá, Paraguay, Asunción, Paraguay (V Bataglia MD); Centro de Pesquisas em Saúde Rerodutiva de Caminas, Caminas, SP, Brazil (A Faundes MD, K Simônia de Pádua BS); EngenderHealth, New York, NY, USA (A Langer MD); Fundación Salud, Ambiente y Desarrollo, Quito, Ecuador (A Narváez MD); Deartment of Eidemiology and Biostatistics, Schulich School of Medicine and Dentistry, University of Western Ontario, London, Ontario Canada (A Donner PhD); CONICET/ Centro de Estudios de Estado y Sociedad, Buenos Aires, Argentina (M Romero MD); The Poulation Council, Latin America Office, Mexico City, Mexico (S Reynoso MD); Karolinska Institutet, Stockholm, Sweden (M Kublickas MD); and Deartment of Obstetrics and Gynaecology, Universidad Nacional de Asunción, Paraguay, Asunción, Paraguay (A Acosta MD) Corresondence to: Dr José Villar Vol 367 June 3, 06 89

2 For the study rotocol and a detailed descrition of the selection rocess see htt:// rovince in Paraguay excluded because did not have facilities for >00 births er year 3 facilities refused to articiate Figure : Trial rofile America; we will reort results of a similar survey done in Africa searately. In 06, we will reare the survey for Asia and Canada. We initially stratified each country by its caital city (always included) and two other randomly-selected administrative geograhic areas (rovinces or states). Within these three areas, we undertook a census of hositals that reorted more than 00 deliveries in the revious year. We then stratified data by rovince or state, choosing a reresentative samle of u to seven institutions each. If there were seven or fewer eligible institutions, we included them all. We included all women admitted to the selected institutions for delivery during a fixed data collection eriod of either 2 or 3 months, deending on the total number of exected deliveries er institution for the comlete year (3 months if 6000 er year; 2 months if >6000 er year). We did not obtain individual informed consent from women, since ours was an institutional-level analysis; we obtained all individual-level data from medical records and did not identify articiants. Institutional informed consent was obtained from the resonsible authority of the articiating health facilities. The ethical committee of WHO and of each country, as well as those of all hositals in Brazil and some of the large hositals in Mexico and Argentina, indeendently aroved the rotocol. 3 countries in America region of 3 randomly selected 8 countries in Latin America included Argentina, Brazil, Cuba, Ecuador, Mexico, Nicaragua, Paraguay, Peru (24 geograhic units, covering the caital city and two randomly selected rovinces in every country) 4 facilities identified in 23 geograhic units 23 facilities randomly selected facilities included (4 facilities with restricted recruitment eriod because of logistical roblems) 2 countries did not articiate Haiti and USA country to start recruitment in 07 Canada Procedures We collected data at two levels institutional and individual. At the institutional level, we gathered data on one occasion only, with the aim of obtaining a detailed descrition of the health facility and its resources for obstetric care. The country or regional coordinator filled in a form during a visit to the institution, in consultation with the hosital coordinator, director, or head of obstetrics. At the individual level, we obtained from all women s medical records information to comlete a two-age re-coded form, summarising obstetric and erinatal events. Trained staff reviewed the medical records of all women within a day after delivery and abstracted data to their individual data collection forms, which were comleted during the eriod that the woman and newborn baby remained in hosital. A nurse or midwife working on the labour or ostartum ward at each institution was resonsible for data collection on a day-to-day basis. A hosital coordinator suervised data collection, resolving or clarifying unclear medical notes before forms were sent for data entry. Attending staff udated incomlete records before discharge. We used the individual-level form to obtain information about demograhic characteristics, maternal risk, regnancy events, mode of delivery, and outcomes u to hosital discharge. The institutional-level form was used to obtain data on characteristics associated with maternal and erinatal care and outcomes, including: laboratory tests; details of anaesthesiology resources; services for intraartum care, delivery, and care of the newborn baby; and resence or absence of basic emergency medical and obstetric care facilities, intensive care units, and human and teaching resources. Criteria for data abstraction were defined in the manual of oerations, 2 which was also available for training staff and monitoring data quality, reducing to a minimum the need for judgment and interretation. The manual contained definitions of all terms used and synonyms of medical and obstetric terms, and described questions and recoded corresonding answers. We retested both data forms in four countries during July and August, 04. We classified caesarean deliveries as: a) emergency, if the woman was referred before onset of labour with a diagnosis of acute fetal distress, vaginal bleeding, uterine ruture, maternal death with fetus alive, or eclamsia; b) intraartum, if indicated during labour, whether labour was sontaneous or induced; c) elective, if decision to do the oeration was made before onset of labour and the woman was referred either from an antenatal clinic or a high-risk ward (if the timing of the decision was unclear, we did not identify as elective those caesareans done in women whose labour had been induced or those done in women who received anaesthetic during a sontaneously initiated labour). We recorded the following erinatal outcomes as otentially affected by caesarean delivery: intraartum 8 Vol 367 June 3, 06

3 fetal death, reterm delivery (<37 weeks), admission to neonatal intensive care unit for 7 days or longer, and neonatal death before hosital discharge of the newborn baby. We assessed maternal morbidity with roxy events, mostly severe conditions, rather than the clinical diagnosis itself, because of roblems in standardising definitions. For examle, we assumed that blood transfusion and hysterectomy indicated severe ostartum haemorrhage; maternal admission to an intensive care unit, maternal death, or maternal hosital stay for longer than 7 days denoted severe comlications. We constructed a summary index severe maternal morbidity and mortality index if at least one of the above comlications was resent and used it as the rimary maternal morbidity outcome. We assessed ostartum treatment with antibiotics (excet rohylactic) searately as an indicator of ostartum infections. Third and fourth degree erine laceration and ostartum fistulae were also maternal outcomes. We classified health institutions as rivate or belonging to the ublic-health system or the social-security system, as reorted by the institutions authorities. We included state university hositals as ublic institutions and all labour-union hositals as social-security institutions. We classified religious institutions according to the atients main mechanism of ayment. Most deliveries in the areas studied are facility-based, with only a small roortion of women having home deliveries. Statistical analysis The rovincial or country coordinator of the survey checked forms for comleteness and accuracy, and any queries were addressed immediately or in consultation with coordinators. We collated all data via the internet at the country coordinator level, using an online data management system based on MedSciNet s clinical trial framework (MedSciNet, Stockholm, Sweden) in collaboration with WHO. We calculated coverage of the survey by comaring the number of forms comleted during the study with the number of deliveries recorded in the logbook of each hosital. Analyses are based on institution-level variables, with individual data aggregated by calculating roortions er institution. We reared a concetual framework to guide data analysis. We develoed a hosital comlexity index, summarising an institution s caacity to rovide different levels of care, deending on its ratings for eight categories: building, general medical care, laboratory, anaesthesiology, screening test, human resources, basic obstetric services, and continuous medical education. For each category, we identified a set of minimum essential services or resources; we classified hositals without any of these services or resources as low level (rating score 0). For most categories, we also identified an additional set of otional services or resources, classifying facilities that had both essential and otional services or resources as high level (rating score 2) and those that were lacking some of the otional services or resources, but had all Proortion caesarean deliveries (%) 80 Intraartum Emergency Elective Public (n=743) 4 Private (n=329) 7 Public (n=2642) Public (n=2643) 4 Private (n=24) 4 Public (n=638) 2 Social security (n=62) 2 Private (n=24) Public (n=799) Social security (n=4628) 2 Private (n=46) Argentina Brazil Cuba Ecuador Mexico Nicaragua Paraguay Peru essentials, as medium level (rating score ). An overall unweighted score (0 6) was calculated for all institutions. We judged hositals with a total score of 9 or less of low comlexity, those with scores of between and 2 of medium comlexity, and those with scores of 3 or more of high comlexity. We recorded institutions as roviding 7 Public (n=342) Social security (n=294) Public (n=2936) Social security (n=89) 3 Public (n=2642) 4 Social security (n=379) Figure 2: Proortion of elective, emergency, and intraartum caesarean deliveries done, according to tye of institution and country Dotted line=median level for all institutions. All (n = 34266) Public (n=2) Social security (n=828) Private (n=296) Cehaloelvic disroortion, dystocia, failure to 26% (8982) 2% (792) 27% (223) 33% (977) rogress Fetal distress % (67) 2% (480) % (646) % (0) Previous caesarean delivery without comlications in 6% () 6% (3627) 3% () 9% (68) current regnancy Previous caesarean delivery with comlications in % (40) 4% (3223) 6% (326) 2% (3) current regnancy Other regnancy comlications 2% (3968) 2% (269) % (84) % (432) Breech or other malresentations % (36) 2% (2647) 9% (778) 7% (9) Pre-eclamsia or eclamsia % (3603) % (2248) 4% (86) 6% (69) Other fetal indications 9% (2926) 9% (999) 9% (7) 6% (76) Other medical comlications 8% (292) 8% (86) 8% (6) % (6) Tubal ligation or sterilisation 6% () 7% (484) 6% (48) 2% (46) Failure to induce labour 4% (292) 4% (804) 4% (366) 4% (22) Intrauterine growth restriction 3% (99) 3% (646) 2% (86) 4% (27) Third trimester vaginal bleeding 3% (864) 3% (76) 3% (22) 2% (63) Multile regnancy 2% (7) 2% (46) 2% (93) 2% (62) Post-term (>42 weeks) 2% (627) 2% (443) 2% (48) % (36) Genital heres or extensive condyloma acuminata <% (2) <% (6) <% (4) <% () Susected or imminent uterine ruture <% (23) <% (7) <% (4) <% (6) Postmortem caesarean section <% (3) <% (2) <% (26) <% (6) HIV ositive <% (26) <% (2) <% () <% (4) Maternal request without any other indication <% (60) <% (3) <% (3) <% (26) Previous reaired fistula <% () <% (2) <% (3) 0 Data are ercentage (number). Sum of ercentages in columns exceeds 0% because some women had multile indications. Table : Indication for caesarean delivery, according to tye of institution For MedSciNet see htt://www.medscinet.com/who For more details of the hosital comlexity index see htt://www.cre.com.ar Vol 367 June 3, 06 82

4 Median (%; th th ercentiles) Previous regnancy Marital status single 4 7 (4 63 0) Age 6 years 4 0 (0 3 8 ) Age 3 years 2 ( 4 7 ) <7 years of education 24 (2 4 7) Primigravidas 34 ( ) Primiarous 4 0 ( 7 0 3) Previous child with low birthweight 3 3 ( 0 6 6) Previous neonatal death or stillbirth 2 ( ) Previous fistula or uterus-cervix surgery 4 6 ( ) Previous caesarean delivery 2 (4 3 6) Current regnancy Any athology before index regnancy* 2 7 (0 4 2 ) Any athology during current regnancy* 3 6 ( ) Gestational hyertension, re-eclamsia, eclamsia 7 ( ) Vaginal bleeding in second half of regnancy 9 ( ) Urinary tract infection ( ) Condyloma acuminate 0 3 (0 0 2) Susected intrauterine growth restriction 0 6 (0 0 3 ) Other medical condition 4 ( 0 9) Any antenatal antibiotic treatment 9 ( ) Birthweight >4 kg 0 40 (0 0 2) Multile regnancy 0 8 (0 0 8) Breech or other non-cehalic resentations 4 3 ( 7 3) Delivery Referred from other institution for regnancy comlications or delivery 8 2 ( ) Induced labour 7 ( 7 2 7) Eidural anaesthesia during labour 3 (0 2) Caesarean delivery in resent regnancy 32 6 ( 7 8) Characteristics of institutions Institutional comlexity index (range 0 6) (8 3) Public 86 (7 7%) Social security 22 (8 3%) Private 2 ( 0%) Economic incentives for caesarean delivery 29 (24%) *Includes athologies of very low incidence not listed indeendently. Data are number (%) of institutions. Table 2: Characteristics of oulations served and health institutions studied an economic incentive to recommend caesarean delivery if they charged their atients fees for delivery and caesarean delivery was either more exensive than vaginal delivery (institutional benefit) or rovided additional income to the senior attending staff (staff benefit). Indicators of the risk of the regnant oulation served by each institution (case mix) included the roortion of women in the institution who: were aged 6 years or younger or 3 years or older; had less than 7 years of education; were single; were rimiarous; had a history of caesarean delivery, stillbirth, or neonatal death; had had surgery on the uterus or cervix; had had a urinary or gynaecological fistula; or had any medical condition diagnosed before the current regnancy. We resent conditions diagnosed during the current regnancy as roortions of women in each institution with a multile regnancy, gestational hyertension, re-eclamsia, eclamsia, vaginal bleeding in the second half of regnancy, condyloma acuminata, HIV, susected imaired fetal growth, or fetal malresentation at term. We also note the roortion of women in each institution who were referred from other institutions, whose labour was induced, and those who received an eidural during labour, all of which we judged risk factors for caesarean delivery. We assessed the crude associations between caesarean delivery and risk factors with the Searman correlation coefficient. For each subgrou of variables related to revious regnancy, current regnancy, and delivery, we fitted a multile linear regression model 22 to the individual factors judged to be associated with caesarean delivery. We considered significant risk factors from these multile regression models as ossible confounders of the association between caesarean delivery and outcomes in further analyses. We then added the hosital comlexity index, tye of institution, and economic incentives for caesarean delivery to the regression models. The association between roortion of caesarean deliveries and maternal and erinatal outcomes was analysed with linear multile regression models, 22 with these outcomes as the deendent variables and the roortion of caesarean deliveries as the main indeendent variable. We describe this relation grahically, using the locally weighted scatter lot smoothing technique (LOWESS). 23 We added risk factors identified in the above algorithm to the models to estimate the indeendent (adjusted) effect of caesarean delivery on maternal and erinatal outcomes. For these analyses, the roortion of outcomes and caesarean deliveries at each institution was transformed to the logit scale, to imrove normality. Role of the funding source External sonsors to WHO for this study had no role in study design, data collection, data analysis, data interretation, or writing of the reort. The corresonding author had full access to all the data in the study and had final resonsibility for the decision to submit for ublication. Results Figure shows the trial rofile. The number of institutions er geograhic region ranged from six in Paraguay to 2 in Mexico; deliveries er country ranged from nearly 300 in Paraguay to in Mexico, and five other countries contributed more than 000 deliveries each to the samle. Most of the health institutions were urban; 0 were tertiary-level, were district hositals, were rimarycare units with surgical facilities, and eight classified as other tye of institution. 40 institutions had or more maternity beds, 44 had 69, and 36 had fewer than. We included all institutions in the regression analyses. The average number of deliveries contributed by 822 Vol 367 June 3, 06

5 Regression coefficient* Previous regnancy Age 6 years % Age 3 years <7 years of education Primiarity <0 000 Caesarean delivery <0 000 Current regnancy Gestational hyertension, re-eclamsia, eclamsia % Vaginal bleeding in second half of regnancy Multile gestation Breech or other non-cehalic resentation Delivery Referred from other institution because of % regnancy comlications or for delivery Eidural during labour Tye of institution Institutional comlexity index < % Economic incentive for caesarean delivery Public Reference Social security Private institutions to the study oulation was similar across countries, ranging from 88 deliveries er hosital in Paraguay to 99 deliveries er hosital in Mexico. The roortion of missing values at the individual level was higher than % only for birthweight of revious infant (23%), maternal height (7%), weight at last renatal visit (%), and number of years of schooling (%). For all the rimary variables caesarean delivery status, birthweight, gestational age, admission of newborn baby to the neonatal intensive care unit, status of baby and mother at discharge, and maternal admission to intensive care the roortion of missing values was less than %. Most of the hositals were of medium comlexity, with a small number having either limited caacity (n=2) or very comlex resources (n=). 2 hositals were rivate, and 86 belonged to the ublic-health system and 22 to the social-security system. Among the 2 rivate institutions, only one had a low comlexity index, comared with three of the 22 social-security institutions and 2 of the 86 ublic-health hositals. Seven of the 2 (8%) rivate institutions had evidence of economic incentives for caesarean delivery, versus % (n= of 22) of the social-security institutions and only 24% (n=2) of ublic hositals. 99% (33 9 of ) of caesarean deliveries and 63% (39 6 of 62 6) of vaginal births were attended by obstetrician gynaecologists or residents. Others were cared for by midwifes, medical or midwife students, general ractitioners, or nurses. 9% of women who needed anaesthetic during labour or delivery were given eidural or sinal rearations (80% of which was rovided by secialists in anaesthesiology). Figure 2 shows caesarean delivery rates according to elective, intraartum, or emergency without labour, study site, and tye of institution. Overall, the median rate of caesarean delivery was 33% (quartile range 24 43); 49% were elective, 46% were intraartum, and % were emergency without labour. The roortion of caesarean delivery was always higher in rivate hositals (median rate %; 43 7) followed by social security and ublic institutions. Higher caesarean delivery rates in rivate and social security institutions were mostly due to an increase in elective caesarean delivery (figure 2). The rate of caesarean delivery among nulliarous women, or those without caesarean delivery in their revious birth, was 68% (n=22 972), ranging from 64% (n=822) in rivate institutions to 69% (n= 768) in ublic ones (not included in the figure). Table shows the indications for caesarean delivery. The most common indication overall was cehaloelvic disroortion/dystocia/failure to rogress. Fetal distress was the second most common indication in ublic and social security institutions, whereas revious caesarean delivery without any comlication in the current regnancy was second in rivate institutions. Overall, % of women undergoing a caesarean delivery had a history of revious caesarean delivery. In social security institutions, reeclamsia or eclamsia was the third most common indication. Tubal ligation or sterilisation was the indication in 6% of the caesarean deliveries at ublic and social security institutions, but in 2% at rivate institutions. Failure of labour induction was an indication for caesarean delivery in about 4% of cases (table ). Among women whose labour was induced, a median of 28% across hositals (quartile range 8 40) went on to have a caesarean delivery. Table 2 shows baseline characteristics and details of regnancy and delivery. Furthermore, in an exloratory analysis, we stratified the results resented in table 2 by rate of caesarean delivery eg, low, medium, or high rate, according to the tertile distribution of caesarean delivery in this samle. We noted no clear risk attern; indeed, hositals with a high rate of caesarean delivery tended to have demograhic and clinical variables suggestive of lower regnancy risk (though rates of revious caesarean delivery concurred with those we reorted). Nevertheless, we adjusted for these baseline variables in all multile regression models included in the tables. Overall, also at the institutional level, maternal and erinatal outcomes were tyical for moderate-risk regnant oulations. The median of the severe maternal morbidity and mortality index in these institutions was 2% (quartile range 4), including haemorrhage with % variance exlained by each model *Obtained with multile linear regression models with resonse variable defined as logit transformation of roortion of caesarean deliveries. All coefficients adjusted by other variables in subgrous. Adjusted for number of variables in model (adjusted R²). Table 3: Association between roortion of risk factors, according to institutions, and roortion of caesarean deliveries (multivariable analysis) Vol 367 June 3,

6 Crude regression coefficient coefficient* coefficient Maternal outcome Severe maternal morbidity and mortality index < Postnatal treatment with antibiotics Perineal laceration or ostartum fistula Perinatal outcome Fetal death Fetal death Neonatal death Neonatal death days on neonatal intensive or secial care unit < days on neonatal intensive or secial care unit Preterm delivery (<37 weeks gestation) < *Adjusted for roortion of rimiarous women, revious caesarean delivery, gestational hyertension or re-eclamsia or eclamsia, referral from other institution for regnancy comlications or delivery, breech or other noncehalic fetal resentation, and eidural during labour. Adjusted for same variables as in * lus comlexity index of institution and tye of institution. Adjusted for same variables as in revious line lus reterm delivery. Table 4: Association between roortion of all caesarean deliveries and maternal and erinatal outcomes at institutional level P Crude regression coefficient coefficient* coefficient Maternal outcome Severe maternal morbidity and mortality index Postnatal treatment with antibiotics Perineal laceration or ostartum fistula Perinatal outcome Fetal death Fetal death Neonatal death Neonatal death days on neonatal intensive or secial care unit days on neonatal intensive or secial care unit Maternal outcome *Adjusted for roortion of rimiarous women, revious caesarean delivery, and breech or other non-cehalic fetal resentation. Adjusted for same variables as in * lus comlexity index of institution and tye of institution. Adjusted for same variables as in revious line lus reterm delivery. Table : Association between roortion of elective caesarean deliveries and maternal and erinatal outcomes at institutional level blood transfusion (0 4%); hysterectomy (0 %), maternal hosital stay of longer than 7 days (0 7%) and maternal death or admission to intensive care (0 2%). The median rate of antibiotic treatment ostnatally was 33% (9 2). Third and fourth degree erineal laceration or ostartum fistula was reorted in a median of 0 2% ( ). The median rate er thousand births of intraartum fetal death was 0 3 ( ), for neonatal death was 4 ( 7), and of staying 7 days or longer in the neonatal intensive care unit was 9 (6 4); the rate of reterm delivery was 6% (4 9). We undertook a multile linear regression analysis, considering the roortion of caesarean deliveries in each institution as the deendent variable, transformed to the logit scale, while considering as indeendent (exlanatory) variables the roortion of regnant women in each institution with the risk factors for caesarean listed in table 2. Primiarity, revious caesarean, re-eclamsia, breech or non-cehalic resentation, referred from other institutions, and eidural anaesthesia in labour were indeendently associated with an increase in caesarean deliveries. Institutions with a high comlexity index, and rivate or social-security institutions were also associated with higher levels of caesarean delivery (table 3). Further adjustments, taking into account the number of deliveries contributed by each hosital, yielded similar results (data not shown). We included variables significantly associated with caesarean delivery in table 3 in a final linear regression model to assess their indeendent effects. The only three criteria that remained ositively significant were rimiarity, caesarean delivery in revious regnancy, and the institutional comlexity index, exlaining 72% of the variance in overall rates of caesarean delivery. We did similar analyses with intraartum and elective caesareans 824 Vol 367 June 3, 06

7 Crude regression coefficient coefficient* coefficient Maternal outcome Severe maternal morbidity and mortality index < < Postnatal treatment with antibiotics Perineal laceration or ostartum fistula Perinatal outcome Fetal death Fetal death Neonatal death Neonatal death days on neonatal intensive or secial care unit < < days on neonatal intensive or secial care unit < Maternal outcome < *Adjusted for roortion of revious caesarean delivery, gestational hyertension or re-eclamsia, or eclamsia, induced labour, and eidural during labour. Adjusted for same variables as in * lus comlexity index of institution and tye of institution. Adjusted for same variables as in revious line lus reterm delivery. Table 6: Association between roortion of intraartum caesarean deliveries and maternal and erinatal outcomes at institutional level as deendent variables. For elective caesarean, only rimiarity and caesarean delivery in revious regnancy remained significant, exlaining 64% of the variation in rates; for intraartum caesarean delivery, revious caesarean section, induction of labour, institutional comlexity, and rivate nature of institution were retained in the final model, exlaining 2% of the variance. What was the association between caesarean delivery and regnancy outcomes after adjustment for oulation risk and institutional characteristics? We used rate of caesarean delivery as the indeendent variable and each maternal and erinatal outcome, both transformed to the logit scale, as deendent variables in searate multile linear regression analyses. In the crude analysis, an increase in rate of caesarean delivery was associated with a significantly higher risk for severe maternal morbidity and mortality and ostnatal treatment with antibiotics (table 4). When adjusted for the set of confounding variables (casemix) and comlexity and tye of institutions, caesarean delivery remained highly significantly associated with an increase in the morbidity and mortality index and in ostnatal treatment with antibiotics (table 4). Rates of third or fourth degree erineal laceration or ostartum fistulae, or both, were not indeendently associated with rates of caesarean delivery. Table 4 also summarises the crude and adjusted association between rate of caesarean delivery and erinatal outcomes. In the crude analysis, caesarean delivery rates were ositively and significantly associated with an increase in the rate of the four negative erinatal outcomes. After adjustment for the case-mix of the oulations served, the rate of caesarean delivery was ositively and statistically associated with an increase in the rates of fetal death, numbers of infants admitted to the neonatal intensive care unit for 7 days or more, and borderline significant for neonatal death after adjusting for reterm delivery. Adjustment for tye of hosital did Adjusted maternal mortality and morbidity index (%, logit scale) 3 0 Adjusted maternal mortality and morbidity index not change these results, although adjustments for comlexity of the institutions eliminated these neonatal negative effects, excet for fetal death (table 4). We stratified the results resented in table 4 by elective and intraartum caesarean delivery. The increase in elective caesareans was ositively and significantly associated with the roortion of women with the severe morbidity and mortality index and ostnatal antibiotic treatment after adjustment for all confounding variables, as in table 4 (table ). Of the erinatal outcomes, only fetal death was indeendently associated with elective caesarean delivery rates. After adjustment for institutional tye and comlexity, the maternal morbidity and mortality index, ostnatal treatment with antibiotics, and fetal death Adjusted ostnatal treatment with antibiotics (%, logit scale) Postnatal treatment with antibiotics Figure 3: Association between rate of caesarean delivery and maternal morbidity and mortality index and ostnatal treatment with antibiotics Rates of outcomes adjusted by roortions of: rimiarous women, revious caesarean delivery, gestational hyertension or re-eclamsia or eclamsia during current regnancy, referral from other institution for regnancy comlications or delivery, breech or other non-cehalic fetal resentation, and eidural during labour, along with comlexity index for institution and tye of institution in multile linear regression analysis. Curves based on LOWESS smoothing alied to scatterlot of logit of rates of caesarean delivery versus logit of adjusted robability of each outcome. Vol 367 June 3, 06 82

8 Adjusted intraartum death (er 00 births, logit scale) 2 7 Intraartum death remained associated with elective caesarean delivery (table ), suggesting that the crude effect of caesarean delivery on neonatal death, rate of infants sending 7 days or more in the neonatal intensive care unit, and reterm delivery is confounded by the oulation characteristics and comlexity of the institution. Table 6 shows a similar analysis as in table, but with intraartum caesarean delivery as the indeendent variable. After adjustment for the same confounding variables, the rate of intraartum caesarean delivery was associated with an increase in the severe maternal morbidity and mortality index, neonatal death, rate of infants sending 7 days or more in the neonatal intensive care unit (even after adjustment for reterm delivery), and total reterm delivery. After adjustment for both the Adjusted neonatal death (er 00 livebirths, logit scale) 2 7 Neonatal death Figure 4: Association between rate of caesarean delivery and intraartum death (er 00 births) and neonatal mortality (er 00 livebirths) Mortality rates adjusted by roortions of: rimiarous women, revious caesarean delivery, gestational hyertension or re-eclamsia or eclamsia during current regnancy, referral from other institution for regnancy comlications or delivery, breech or other non-cehalic fetal resentation, and eidural during labour, along with comlexity index for institution and tye of institution in multile linear regression analysis. Adjusted stay in neonatal intensive care unit for 7 days (%, logit scale) Stay in neonatal intensive care unit for 7 days Adjusted reterm delivery (%, logit scale) Preterm delivery Figure : Association between rate of caesarean delivery and neonatal admission to intensive care for 7 days or more and reterm delivery Rates of outcomes adjusted by roortions of: rimiarous women, revious caesarean delivery, gestational hyertension or re-eclamsia or eclamsia during current regnancy, referral from other institution for regnancy comlications or delivery, breech or other non-cehalic fetal resentation, and eidural during labour, along with comlexity index for institution and tye of institution in multile linear regression analysis. tye of institution and institutional comlexity, the severe maternal morbidity and mortality index and rate of infants sending 7 days or more in the neonatal intensive care unit remained ositively and significantly associated with rate of intraartum caesarean delivery. Finally, we assessed whether there was a threshold rate of caesarean delivery associated with the noted increase in negative outcomes, as adjusted for the confounding variables considered in table 4. For ostnatal maternal treatment with antibiotics and severe maternal morbidity and mortality index, the increase seemed linear (figure 3). Risk of reterm delivery and neonatal death rose at caesar ean delivery rates of between % and % (figures 4 and ). Discussion Our findings indicate that increase in rates of caesarean delivery is associated with increased use of antibiotics ostartum, greater severe maternal morbidity and mortality, and higher fetal and neonatal morbidity, even after adjustment for demograhic characteristics, risk factors, general medical and regnancy associated comlications, tye and comlexity of institution, and roortion of referrals. The high rates of caesarean delivery and its more frequent indications were similar across countries with different health systems and erinatal outcomes. Our study had limitations, including the ossibility of selection bias. Sources could result from the inability of three of the original selected countries to articiate in a timely fashion, the refusal of three selected institutions to articiate, and the deterministic selection of the caital cities in each country. Furthermore, the large number of health institutions involved limited standardisation of diagnoses. We therefore concentrated our analyses on a few unequivocal morbidity and mortality indicators, using data rosectively abstracted by staff from the same hosital; we discussed unclear or incomlete records directly with the attending medical staff. Additionally, our real-time, web-based data entry system and its internal consistency rocedures facilitated the identification of incomlete or inconsistent data, which could then be queried within a few weeks of the event. For logistical reasons, the survey lasted only 3 months, and so did not cature ossible time-related effects eg, in the characteristics of the oulation or relating to training of new staff. Our analyses and inferences are based on institutional-level data, for the urose of making institutional-level recommendations. The so-called ecological fallacy 24 does not, therefore, aly here. Although we have made extensive statistical adjustments for many ossible confounding variables, unidentified factors might have affected our noted associations. The consistent trends noted are, however, unlikely to have been affected in such a way. Finally, the very high rates of caesarean delivery observed in this survey may not be directly extraolated to the whole country or region, but should reflect very well the situation in large institutions in 826 Vol 367 June 3, 06

9 these countries. We also believe that the relationsshis with outcomes we have succeeded in identifying should be generalisable beyond the articiating institutions. Indeendent of mothers risk, use of eidural in labour, or tye and comlexity of institution, high rates of caesarean delivery were associated at the institutional level with ostnatal treatment with antibiotics, in addition to the rohylactic antibiotics recommended after caesarean delivery. These findings concur with the increased level of infections associated with caesarean delivery in hositals in develoed countries. 2 Caesarean delivery rates were also indeendently associated with the maternal morbidity and mortality index, which included conditions such as blood transfusions in agreement with reorted higher risk of caesarean delivery for severe ostartum haemorrhage 26 and the roortion of women who stayed in hosital for more than 7 days ostartum ie, beyond the maximum stay for uncomlicated caesarean delivery. Also, rates of caesarean delivery were not associated with a rotective effect on erineal lacerations, as could have been exected. Caesarean delivery did not imrove erinatal outcomes either, as suggested by data from develoed countries. 27 On the contrary, an increase in fetal death was indeendently associated with caesarean delivery, esecially elective caesarean delivery. This finding is difficult to interret, since we did not record the recise timing of death vis-à-vis the indication for caesarean, although elective caesarean delivery is usually not indicated for stillbirths. However, similar observations have been made in high-risk women who had had a revious caesarean (the most common indication for caesarean delivery in our oulation) 28 and among obstetricians in the USA with high rates of caesarean delivery, who also recorded higher rates of fetal death among low birthweight infants than obstetricians with lower rates of caesarean deliveries. 27 Our original hyothesis was that rates of caesarean delivery would show a U-shaed association with negative erinatal outcomes. We did not note such a attern, even in the adjusted analysis, erhas because there were only a few hositals with low rates of caesarean delivery. We did note an increased risk of reterm delivery and neonatal mortality starting between rates of caesarean delivery of % and %. The higher rates of newborn babies sending 7 days or more in a neonatal intensive care unit among hositals with high caesarean delivery rates could be related to an increase in resiratory distress syndrome associated with elective caesarean delivery. Rates of caesarean delivery, esecially elective caesarean delivery in rivate hositals, reflect a comlex social rocess, affected by clinical status, family and social ressures, the legal system, availability of technology, women s role models (celebrity elective caesarean delivery). Examles from rivate institutions show that moderate rates of caesarean delivery are not unrealistic even in affluent societies. 29 Our results also show how a medical intervention or treatment that is effective when alied to sick individuals in emergency situations can do more harm than good when alied to healthy oulations. In Latin America, about million babies are born every year. An increase from % (as initially suggested) to the observed 3% in caesarean deliveries, reresents an additional 2 million caesarean deliveries er year. The difference in cost (without any comlications of caesarean delivery) between a vaginal delivery and a caesarean delivery is about US$30 for a country like Chile. In a develoed country, for each % increase in caesarean deliveries, there is an increase in cost of about US$9 million. 3 These large sums of money could be used to imrove other areas of maternal and newborn care and to ay for needed research. In conclusion, high rates of caesarean delivery do not necessarily indicate good quality care or services. Indeed institutions that deliver a lot of babies by caesarean should initiate a detailed and rigorous assessment of the factors related to their obstetric care and the erinatal outcomes achieved vis-à-vis the case mix of the oulation they serve; at resent their services might cause (iatrogenic) harm. Contributors J Villar, G Carroli, A Faundes, A Donner, L Bakketeig, and A Shah were resonsible for the idea and concetion of the survey. J Villar, A Shah, G Carroli, and A Donner reared the rotocol. L Camodónico, G Carroli, J Villar, and A Shah suervised and coordinated the survey s overall undertaking in Latin America. D Wojdyla, L Camodónico, A Donner, D Giordano, and M Kublickas were resonsible for data management and analysis in collaboration with J Villar. E Valladares, N Zavaleta, A Velazco, V Bataglia, A Langer, A Narváez, M Romero, S Reynoso, K Simônia de Pádua, and A Acosta collaborated in the rearation of the rotocol and the survey and imlemented it in their resective countries. They actively contributed to the overall undertaking of the trial. J Villar, G Carroli, A Donner, and A Faundes wrote the reort with inut from all investigators. All investigators read the reort and made substantive suggestions on its content. 0 WHO global survey committees Steering committee A Faundes (chairman), L S Bakketeig, E O Akande, A Kosia, A Langer, G Carroli, P Lumbiganon, D Oluwole, and M Lydon-Rochelle. Ex officio: J Villar, A Shah. Survey coordinating unit for Latin America G Carroli (regional coordinator), L Camodónico (regional data manager), D Giordano, J Villar, A Shah. Data analysis sub-committee D Wojdyla, J Villar, A Donner, M Taljaard, L Camodónico, F Burgueño, R Zanello. Country collaborators Argentina M Romero, M Molinas, B Petz; R Votta, R Winograd, S Bulacio (Hosital General de Agudos Cosme Argerich ); P Saosnik, N J Bruno, L Acuña, M Pared, G Perez Giambriani (Hosital General de Agudos José María Penna ); P Justich, R Luca, S Mazzeo, M Marinelli (Hosital General de Agudos Donación F Santojanni); J D Argento, L Flores, MV Secondi (Hosital Materno Infantil Ramón Sarda); J Falcón, A Brondolo, G Musante (Clínica y Maternidad Suizo Argentina); A Lambierto, J Pascual, H Bergondo, L Bouyssounadea Agüero (Sanatorio Otamendi); H Marchitelli, L Otaño, M Sebastiani, J Ceriani Cernadas, J Saadi (Hosital Italiano); R Rizzi; M E Jofre, D Cerda, M F Rizzi (Hosital Universitario de Maternidad y Neonatología); H E Bolatti, L M Ramallo, J Mainguyague, F Creso Roca (Hosital Materno Neonatal); M J Figueroa, J M Olmas, E Villar, J Oviedo, Z Maldonado, V González, M I Viale, P Feier, L Rodriguez, F Rolon, C Barbieri, M García Salguero (Hosital Materno Provincial); F Andion, P Panzeri (Hosital Misericordia); J Nores Fierro, M Jofre, D Santoni, I Maggi, F Bazan Flett, S Aodassio, L Ret Davalos, Vol 367 June 3,

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